John E. Layne

The visual control of behaviour in fiddler crabs

The distribution of resolution around the eye of the fiddler crab Uca pugilator was measured using the pseudopupil, and the results were compared with various behavioural thresholds. As noted previously (Zeil et al. 1986) the eye has a band of greatly increased vertical resolution around the middle with inter-ommatidial angles as small as 1° (Figs. 1–3). In life this band images the horizon. The horizontal resolution is nearly constant throughout the eye. Males notice females when they subtend 2 to 3 inter-ommatidial angles, and distinguish males from females when they subtend 6 to 7 ommatidia (Fig. 6). Potential predators are detected when they subtend only one inter-ommatidial angle, and move through a similar angle. Using models, it was found that males respond to moving objects of the right size as though they were conspecifics, although they do not resemble crabs in shape. It is concluded that only one feature distinguishes other crabs from predators: whether they appear below or above the crabs horizon.

Mechanisms of homing in the fiddler crab Uca rapax 2.Information sources and frame of reference for a path integration system

SUMMARY Fiddler crabs Uca rapax are central-place foragers, making feeding excursions of up to several meters from their burrows. This study investigates the sources of directional and distance information used by these crabs when returning to their burrows. We tested the spatial frame of reference (egocentric or exocentric), and the source of spatial information (idiothetic or allothetic) used during homing. We also tested which components of their locomotion they integrated (only voluntary, or voluntary plus reflexive). Fiddler crabs in their natural mudflat habitat were passively rotated during normal foraging behavior using experimenter-controlled disks, before they returned home. Crabs resisted passive rotations on the disk by counter-rotating when the disk turned, which was a compensatory response to unintended movement. Crabs were usually situated eccentrically on the disk, and therefore were also subjected to a translation when the disk rotated. No crab actively compensated for this translation. Crabs that fully compensated for disk rotation made no directional homing error. Crabs that did not fully compensate homed in a direction that reflected their new body orientation. In other words, if we succeeded in reorienting a crab (i.e. it undercompensated for disk rotation), its homing error was equal to the angle by which it had been reoriented, regardless of the magnitude of the optomotor compensation. Computer-modelled crabs, each equipped with a path integrator utilizing different combinations of external (allothetic) and path-related (idiothetic) input, traversed the digitized paths of the real crabs. The home vector computed by the model crab was then compared to the homing direction observed in the real crab. The model home vector that most closely matched that of the real crab was taken to comprise the path integration mechanism employed by fiddler crabs. The model that best matched the real crab gained direction and distance idiothetically (from internal sources such as proprioceptors), and integrated only voluntary locomotory information. Crabs were also made to run home across a patch of wet acetate, on which they slipped and were thus forced to take more steps on the homeward path than theoretically required by the home vector. Crabs whose running velocity across the patch was unusually low also stopped short of their burrow before finding it. Crabs whose running velocity was not impeded by the patch did not stop short, but ran straight to the burrow entrance, as did control crabs that ran home with no slippery patch. We interpret this to mean that the velocity of some crabs was impeded because of slipping, and these therefore stopped short of their burrow after having run out their homing vector. This is positive evidence in support of the hypothesis that path integration is mediated either by leg proprioceptors or by efferent commands, but our data do not allow us to distinguish between these two possibilities.

Fiddler Crabs Use the Visual Horizon to Distinguish Predators from Conspecifics: A Review of the Evidence

Male fiddler crabs, Uca pugilator (Crustacea: Decapoda), respond to conspecifics by claw waving, and to predators by freezing or escape. In field experiments it was found that this distinction was not made on the basis of angular size and speed, nor was shape important. The remaining possibilities were either the absolute size of the stimulus, determined from angular size and distance, or the position of the stimulus relative to the horizon. To distinguish between these, a crab was placed in a glass dish, and moved black stimuli on a white background, at a distance of 22 cm. Stimuli below the crabs horizon hardly ever evoked escape. However, identical stimuli partially or wholly above the crabs horizon produced escape responses whose frequency varied with the angular size of the stimulus. Halving the distance of the stimulus showed that it was angular and not absolute size that determines escape frequency; and experiments with a tilted horizon showed that it is the position of the stimulus relative to the eye equator that is important, rather than the geographical horizon itself. It has been concluded that crabs categorize stimuli as dangerous or otherwise by their position relative to the crabs’ visual horizon.

Molecular evidence for color discrimination in the Atlantic sand fiddler crab, Uca pugilator

SUMMARY Fiddler crabs are intertidal brachyuran crabs that belong to the genus Uca. Approximately 97 different species have been identified, and several of these live sympatrically. Many have species-specific body color patterns that may act as signals for intra- and interspecific communication. To understand the behavioral and ecological role of this coloration we must know whether fiddler crabs have the physiological capacity to perceive color cues. Using a molecular approach, we identified the opsin-encoding genes and determined their expression patterns across the eye of the sand fiddler crab, Uca pugilator. We identified three different opsin-encoding genes (UpRh1, UpRh2 and UpRh3). UpRh1 and UpRh2 are highly related and have similarities in their amino acid sequences to other arthropod long- and medium-wavelength-sensitive opsins, whereas UpRh3 is similar to other arthropod UV-sensitive opsins. All three opsins are expressed in each ommatidium, in an opsin-specific pattern. UpRh3 is present only in the R8 photoreceptor cell, whereas UpRh1 and UpRh2 are present in the R1-7 cells, with UpRh1 expression restricted to five cells and UpRh2 expression present in three cells. Thus, one photoreceptor in every ommatidium expresses both UpRh1 and UpRh2, providing another example of sensory receptor coexpression. These results show that U. pugilator has the basic molecular machinery for color perception, perhaps even trichromatic vision.

Spectral sensitivity of the principal eyes of sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae), larvae.

SUMMARY The principal eyes of sunburst diving beetle, Thermonectus marmoratus, larvae are among the most unusual eyes in the animal kingdom. They are composed of long tubes connecting bifocal lenses with two retinas: a distal retina situated a few hundred micrometers behind the lens, and a proximal retina that is situated directly beneath. A recent molecular study on first instar larvae suggests that the distal retina expresses a long-wavelength-sensitive opsin (TmLW), whereas the proximal retina predominantly expresses an ultraviolet-sensitive opsin (TmUV II). Using cloning and in situ hybridization we here confirm that this opsin distribution is, for the most part, maintained in third instar larvae (with the exception of the TmUV I that is weakly expressed only in proximal retinas of first instar larvae). We furthermore use intracellular electrophysiological recordings and neurobiotin injections to determine the spectral sensitivity of individual photoreceptor cells. We find that photoreceptors of the proximal retina have a sensitivity curve that peaks at 374–375 nm. The shape of the curve is consistent with the predicted absorbance of a single-opsin template. The spectral response of photoreceptors from the distal retina confirms their maximum sensitivity to green light with the dominant λ-peak between 520 and 540 nm, and the secondary β-peak between 340 and 360 nm. These physiological measurements support molecular predictions and represent important steps towards understanding the functional organization of the unusual stemmata of T. marmoratus larvae.

Behavioral evidence for within-eyelet resolution in twisted-winged insects (Strepsiptera)

SUMMARY Compound eyes are typically composed of hundreds to thousands of ommatidia, each containing 8–10 receptors. The maximal spatial frequency at which a compound eye can sample the environment is determined by the inter-ommatidial angle. Males of the insect order Strepsiptera are different: their eyes are composed of a smaller number of relatively large units (eyelets), each with an extended retina. Building on a study of Xenos vesparum, we use a behavioral paradigm based on the optomotor response to investigate the possibility that the eyelets of the Strepsiptera Xenos peckii are image-forming units. From anatomical evidence, we hypothesize that spatial sampling in the strepsipteran eye is determined not only by the interactions of widely spaced photoreceptors in different eyelets, but also by the angular separation between groups of closely spaced photoreceptors within eyelets. We compared X. peckiis optomotor response with the predictions of an elementary motion detector (EMD) model consisting of two distinctly different sampling bases. The best match between our empirical results and the model shows that the optomotor response in X. peckii males is determined by both the small (intra-eyelet) and large (possibly inter-eyelet) separations. Our results indicate that the X. peckii eye has sampling bases around 10° and 20°, and that each eyelet could be composed of up to 13 sampling points, which is consistent with previous anatomical findings. This study is the first to use the EMD model explicitly to investigate the possibility that strepsipteran eyes combine motion detection features from both camera and compound eyes.

Fiddler crabs accurately measure two-dimensional distance over three-dimensional terrain.

SUMMARY Foraging fiddler crabs (Uca spp.) monitor the location of, and are able to return to, their burrows by employing path integration. This requires them to accurately measure both the directions and distances of their locomotory movements. Even though most fiddler crabs inhabit relatively flat terrain, they must cope with vertical features of their environment, such as sloping beaches, mounds and shells, which may represent significant obstacles. To determine whether fiddler crabs can successfully perform path integration among such three-dimensional obstacles, we tested their ability to measure distance while we imposed a vertical detour. By inserting a large hill in the homeward path of foraging crabs we show that fiddler crabs can cope with vertical detours: they accurately travel the correct horizontal distance, despite the fact that the shape of the hill forces them to change their gait from what would be used on flat ground. Our results demonstrate a flexible path integrator capable of measuring, and either integrating or discarding, the vertical dimension.

Population differences in olfaction accompany host shift in Drosophila mojavensis.

Evolutionary shifts in plant–herbivore interactions provide a model for understanding the link among the evolution of behaviour, ecological specialization and incipient speciation. Drosophila mojavensis uses different host cacti across its range, and volatile chemicals emitted by the host are the primary cue for host plant identification. In this study, we show that changes in host plant use between distinct D. mojavensis populations are accompanied by changes in the olfactory system. Specifically, we observe differences in olfactory receptor neuron specificity and sensitivity, as well as changes in sensillar subtype abundance, between populations. Additionally, RNA-seq analyses reveal differential gene expression between populations for members of the odorant receptor gene family. Hence, alterations in host preference are associated with changes in development, regulation and function at the olfactory periphery.

Evolution of coeloconic sensilla in the peripheral olfactory system of Drosophila mojavensis

Populations inhabiting habitats with different environmental conditions, such as climate, resource availability, predation, competition, can undergo selection for traits that are adaptive in one habitat and not the other, leading to divergence between populations. Changes in the olfactory systems of insects that rely on different host plants, for example, can occur in response to differences in sensory stimuli between habitats. In this study, we investigate the evolution of host preference by characterizing the coeloconic sensilla in Drosophila mojavensis, a species that breeds on different necrotic cacti across its geographic range. These cactus species differ in the volatile chemicals they emit, a primary sensory cue for host plant discrimination. Analysis of odor-evoked responses identified four coeloconic sensilla that were qualitatively similar to those of Drosophila melanogaster, but varied in the breadth and strength of their olfactory sensory neuron responses to some acids and amines. Variation in responses to certain odorants among D. mojavensis populations was also observed. Compared to D. melanogaster, there was a lack of sensitivity of antennal coeloconic type 3 (ac3) sensilla to primary ligands of OR35a across all populations. Consistent with this result was a lack of detectable Or35a gene expression. Using a comparative approach, we then examined odor specificity of ac3 sensilla for seven additional Drosophila species, and found that OR35a-like sensitivity may be limited to the melanogaster subgroup. The variation in specificity that was observed among species is not clearly attributable to the degree of ecological specialization, nor to the ecological niche.

Correction to ‘Population differences in olfaction accompany host shift in Drosophila mojavensis ’

Evolutionary shifts in plant–herbivore interactions provide a model for understanding the link among the evolution of behaviour, ecological specialization and incipient speciation. Drosophila mojavensis uses different host cacti across its range, and volatile chemicals emitted by the host are the primary cue for host plant identification. In this study, we show that changes in host plant use between distinct D. mojavensis populations are accompanied by changes in the olfactory system. Specifically, we observe differences in olfactory receptor neuron specificity and sensitivity, as well as changes in sensillar subtype abundance, between populations. Additionally, RNA-seq analyses reveal differential gene expression between populations for members of the odorant receptor gene family. Hence, alterations in host preference are associated with changes in development, regulation and function at the olfactory periphery.